Selective Targeting of the Dendrites of Corticothalamic Cells by Thalamic Afferents in Area 17 of the Cat

Abstract

Pyramidal cells of layer 6 in cat visual cortex are the source of the corticothalamic projection, and their recurrent collaterals provide substantially more excitatory synapses in layer 4 than does the thalamic input. They have predominantly simple receptive fields and can be driven monosynaptically by electrically stimulating thalamic relay cells. Layer 6 cells could thus provide a significant disynaptic amplification of the thalamic input to layer 4, particularly since their synapses facilitate, unlike the thalamic afferents whose synapses depress. However, purely geometric considerations of the relation of their dendritic trees to the thalamic input indicate that they should form a far smaller number of synapses with thalamic afferents than do the simple cells of layer 4. We thus analyzed quantitatively the thalamic input to identified corticothalamic cells by labeling the thalamic afferents and corticothalamic cells in vivo. We made a correlated light and electron microscopic study of 73 "contacts" between thalamic afferents and five corticothalamic cells. The electron microscope revealed that only 24 of the contacts identified at light microscope level were indeed synapses and, contrary to geometric predictions, virtually all were located on spines on the basal dendrites. Our quantitative estimates indicate that the corticothalamic cells form even fewer synapses with the thalamic afferents than predicted by geometric considerations and only 1/10 as many as do the layer 4 simple cells. These data strongly suggest it is the collective computation of cortical neurons, not the monosynaptic thalamic input, that determines the output of the corticothalamic cells.

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

“…Although occasional retrogradely labeled corticothalamic cells were seen (da Costa and Martin, 2009b), none were located in the proximity of the SS used in this study. Moreover, none of the axons contacting the SS resemble those of layer 6 pyramidal cells, which are studded with small bouton terminaux (Martin and Whitteridge, 1984;McGuire et al, 1984).…”

“…Given the number of the thalamic synapses per neuron and the number of dendritic branches, it is statistically bound to happen that several thalamic synapses share the same dendritic segment and interact, but this appears not to be a fundamental design principle. In our study of thalamic connectivity with corticothalamic neurons (da Costa and Martin, 2009b), multiple synapses from the same axon were formed with the same dendritic segment. Here we never detected multiple synapses on a dendrite from a single axon despite the fact that SSs are surrounded by a much higher density (ϳ10ϫ) (Humphrey et al, 1985) of thalamic boutons than are the layer 6 corticothalamic neurons.…”

“…Such structural features include a proximal position on the dendritic tree, cooperative clustering of thalamic synapses, the large size of the synapses, multiple synapses made by a single axon with its target cells [as in the retinogeniculate projection (Hamos et al, 1987) and some targets of the thalamocortical pathway (Freund et al, 1985b;da Costa and Martin, 2009b)], and whether the targets, which are mainly spines, have any characteristics that might facilitate or augment synaptic current flow. Physiological studies indicate that virtually all neurons in layer 4 can be driven monosynaptically from the dLGN, which implies that all simple cells receive a similar weight of input from dLGN.…”

The Synaptic Organization of the Claustral Projection to the Cat's Visual Cortex

“…50/3002 to K.A.C.M. Details of the anesthetics and surgical operation have been reported previously (da Costa and Martin, 2009b).…”

Properties of Layer 6 Pyramidal Neuron Apical Dendrites

“…d, Peak amplitudes of ⌬F/F as a function of the time interval between the extracellular stimulation and the train of somatic APs (⌬t) for the example shown in a-c. Measurements were obtained in control conditions (red) and in the presence of the GABA B antagonist CGP 52432 (1 M; blue) and after further addition of the GABA A antagonist gabazine (GBZ; 3 M; black). e, Average inhibition curve for five cells as in d. Costa and Martin, 2009). This highlights the need for close investigation of all connectivity with regard to which part of the dendritic tree is contacted.…”